Layer-specific strain and dyssynchrony index alteration in new-onset systemic lupus erythematosus patients without cardiac symptoms
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Original Article
Layer-specific strain and dyssynchrony index alteration in
new-onset systemic lupus erythematosus patients without cardiac
symptoms
Tingting Luo1#, Zhenhua Wang2#, Zhen Chen3, Ermei Yu1, Chenglong Fang3
1
Department of Echocardiography, Second Affiliated Hospital of Fujian Medical University, Quanzhou, China; 2Department of Cardiology, Second
Affiliated Hospital of Fujian Medical University, Quanzhou, China; 3Department of Rheumatology, Second Affiliated Hospital of Fujian Medical
University, Quanzhou, China
#
These authors contributed equally to this work.
Correspondence to: Chenglong Fang. Department of Rheumatology, Second Affiliated Hospital of Fujian Medical University, Donghai Avenue 950,
Quanzhou 362000, China. Email: fangcl900523@126.com.
Background: Layer-specific speckle-tracking echocardiography (STE) is a noninvasive approach that
assesses subclinical left ventricular dysfunction. We aimed to investigate the (I) alteration of layer-specific
STE parameters and the dyssynchrony index; and (II) the disease parameters associated with layer-specific
STE change in drug-naïve patients with new-onset systemic lupus erythematosus (SLE) without cardiac
symptoms.
Methods: Thirty-five drug-naïve patients with new-onset SLE and twenty-five healthy controls were
enrolled. All individuals received both conventional echocardiographic and two-dimensional STE
assessment. The data of layer-specific global longitudinal strain (GLS), global circumferential strain (GCS),
and peak systolic dispersion (PSD) were acquired in layer-specific STE.
Results: All patients had a normal left ventricular ejection fraction (LVEF)(mean LVEF: 58%) and
conventional echocardiographic parameters were comparable between patients and controls. Decreased
layer-specific GLS and elevated PSD were observed in SLE patients (whole layer GLS: −17.6%±3.0% versus
−19.3%±2.6%, P=0.02; endocardial GLS: −20.0%±3.2% versus −22.1%±3.0%, P=0.01; epicardial GLS:
−15.6%±2.7% versus −16.8%±2.4%, P=0.04; PSD: 41.0±18.9 versus 28.8±10.1 msec, P=0.007). In contrast,
there was no difference in layer-specific GCS at three different levels between patients and controls (P>0.05).
More severely impaired GLS was observed in patients with higher disease activity, high-risk antiphospholipid
antibody (aPL) profile, or renal involvement. The PSD was increased in patients with higher disease activity
or a high-risk aPL profile. Correlational analysis showed that GLS at three layers and PSD correlated with
high-sensitivity C-reactive protein (hsCRP) levels (whole GLS: r=0.662, P
1272 Luo et al. Layer-specific speckle-tracking scan in SLE patients
Submitted Jul 13, 2020. Accepted for publication Oct 26, 2020.
doi: 10.21037/qims-20-859
View this article at: http://dx.doi.org/10.21037/qims-20-859
Introduction 2020. All patients fulfilled the 2012 American College
of Rheumatology (ACR)/Systemic Lupus International
With advances in immunosuppressive therapies, the short-
Collaborating Clinics (SLICC) criteria (10). The onset of
term outcome of patients with systemic lupus erythematosus
SLE-related symptoms occurred within 1 month prior to
(SLE) has significantly improved. However, SLE patients
study entry, and patients had no cardiac symptoms. Disease
have up to a 10-fold increased risk of cardiovascular
activity was assessed by the Systemic Lupus Erythematosus
morbidity and mortality, and cardiac involvement still
Disease Activity Index-2K (SLEDAI-2K). The high-risk
accounts for most deaths (1). Cardiac impairment in SLE is
antiphospholipid antibody (aPL) profile was defined as
often asymptomatic and not always in parallel with disease
the presence of lupus anticoagulant, or of double or triple
activity (2,3). While transthoracic echocardiography is a
aPL positivity, or the presence of persistently high aPL
routine method to screen cardiovascular system involvement
titres (11). A group of healthy controls included age-
in SLE, it often fails to detect subclinical ventricular
matched volunteers with a negative result to antinuclear
dysfunction for several reasons. For example, abnormal left
antibodies and no history of systemic disease was also
ventricular ejection fraction (LVEF) tends to reflect global
established. Other inclusion criteria for this group were
but not regional myocardial dysfunction. Furthermore,
normal echocardiography, electrocardiographic, N-terminal
disadvantages including load and angle dependency and low
pro-B-type natriuretic peptide (NT-proBNP), and troponin
reproducibility exist in the measurement of LVEF (4).
I results. Exclusion criteria included age
Quantitative Imaging in Medicine and Surgery, Vol 11, No 4 April 2021 1273
and trans-mitral peak velocity of late diastole, respectively. summarized in Table 1. A total of 35 SLE patients with new-
Left ventricular diastolic function was assessed according onset disease and 25 healthy controls were enrolled. Stable-
to the 2016 American Society of Echocardiography/ to-mild disease activity was found in 51% of patients (n=18),
European Association of Cardiovascular Imaging while 40% had moderate disease activity (n=14), and 9%
recommendations (12). In patients with normal LVEF, the had high disease activity (n=3). No cardiac symptoms were
four variables for identifying diastolic dysfunction, and reported in either SLE patients or controls. All participants
their abnormal cutoff values were the following: septal e’ had normal serum markers of cardiac injury including
34 mL/m2, and peak TR velocity >2.8 m/sec. and troponin I, indicating an absence of clinical evidence of
cardiac impairment in the SLE patients.
2D STE assessment
Conventional echocardiographic parameters
Two-dimensional STE was performed using a GE VIVID
E95 ultrasound system. Images of the apical four-chamber, Conventional echocardiographic results are summarized in
apical two-chamber, apical LV long-axis, and LV short- Table 2. All participants had normal LVEF. No significant
axis views at the basal, papillary, and apical levels were differences of parameters assessing systolic and diastolic
collected within 3–5 cardiac cycles. The software package function including LVEDV, LVESV, LVEDD, LVESD,
EchoPAC (version 201 6.3, GE Vingmed Ultrasound) was IVS, PWT, E, A, septal e’, lateral e’, averaged e’, E/e’, TR
used to analyze images. Software tracked the endocardium velocity, or LAVI were found between SLE patients and
outline and divided the whole ventricle wall into three healthy controls (P>0.05, all).
layers (an endocardial, a mid-myocardial and an epicardial
layer). Quantitative myocardial parameters for the global Layer-specific STE characteristics, left ventricular
longitudinal strain (GLS) and global circumference strain dyssynchrony index (PSD), and disease parameters in SLE
(GCS) of each layer, and PSD, were obtained. STE data patients
analyses were conducted by two investigators (TL and ZW)
who had experience with layer-specific STE and were blind The representative images of layer-specific STE’s of
to the clinical data. one SLE patient and one healthy control are shown in
Figures 1 and 2 respectively, and the results of layer-
specific STE parameters are displayed in Table 3. Although
Statistical analysis clinical evidence of cardiac involvement was not detected
Differences and correlations between patients and controls in SLE patients through routine assessment, an increase
were analyzed using t-test and Pearson’s correlation analysis, in impairment of left ventricular GLS at three layers
respectively, when the data was normally distributed. When (whole layer GLS, endocardial GLS, and epicardial GLS)
it was not, the nonparametric Mann-Whitney rank-sum test was observed in drug-naïve patients with new-onset SLE,
and Spearman’s correlation analysis were applied. Partial compared with controls (P=0.02, 0.01, 0.04, respectively).
Elevation of PSD, which reflects left ventricular
correlation analysis and multivariate linear regression
dyssynchrony, was also found in SLE patients (P1274 Luo et al. Layer-specific speckle-tracking scan in SLE patients Table 1 Characteristics of SLE patients and controls Variables SLE (n=35) Healthy controls (n=25) P Female/male 29/6 20/5 0.778 Age (years) 33±6 32±6 0.863 Immune parameters Serum C3, gm/liter 0.62±0.18 1.13±0.08
Quantitative Imaging in Medicine and Surgery, Vol 11, No 4 April 2021 1275
Table 2 Conventional and TDI echocardiographic parameters in SLE patients and controls
Variables SLE (n=35) Healthy controls (n=25) P
LVEDV (mL) 94.4±13.4 92.5±16.8 0.553
LVESV (mL) 39.6±6.4 37.6±7.0 0.337
LVEDD (mm) 45.8±2.5 45.6±3.3 0.838
LVESD (mm) 31.6±1.9 31.4±2.8 0.915
IVS (mm) 9.4±0.8 9.6±0.7 0.340
PWT (mm) 8.9±0.7 9.1±0.9 0.360
E (cm/s) 88.0±11.3 90.2±11.6 0.553
A (cm/s) 59.5±11.3 62.4±9.1 0.162
Septal e’ (cm/s) 10.7±2.0 11.1±1.9 0.429
Lateral e’ (cm/s) 13.5±1.7 13.7±1.7 0.656
Averaged e’ (cm/s) 12.3±1.7 12.2±1.8 0.863
E/e’ 7.2±0.7 7.4±0.7 0.163
TR velocity (m/s) 2.4±0.2 2.3±0.2 0.377
2
LAVI (mL/m ) 25.1±3.8 25.8±3.7 0.479
LVEDV, left ventricular end-diastolic volume; LVESV, left ventricular end-systolic volume; LVEDD, left ventricular end-diastolic diameter;
LVESD, left ventricular end-systolic diameter; IVS, interventricular septum; PWT, posterior wall thickness; E, transmitral peak velocity
of early diastole; A, transmitral peak velocity of late diastole; e’, velocity of early diastole of the mitral annulus; TR velocity, tricuspid
regurgitation velocity; LAVI, left atrial volume index.
higher disease activity or high-risk aPL, but not in those Discussion
with lupus nephritis (Table 4).
In 2016, Ozawa et al. first analyzed the relationship
Correlation analysis showed that endocardial GLS, whole
between layer-specific strain parameters and heart failure
layer GLS, epicardial GLS, and PSD correlated with high-
indicators in 20 systemic autoimmune disorder patients,
sensitivity CRP (hsCRP) levels in SLE patients, but not in
including 7 SLE patients. They found that GCS values,
healthy controls. PSD also correlated with the three layer-
but not GLS in whole, endocardial, or epicardial layers,
specific GLS parameters above (Figure 3). Partial correlation correlated with serum B-type natriuretic peptide (BNP)
analysis showed that PSD correlated with epicardial GLS, levels (13). In addition, GCS in the endocardial layer was
but not with whole layer GLS or endocardial GLS, when significantly positively correlated with LVEF. To the best
treating hsCRP level, renal involvement, aPL profile, and of our knowledge, the present study is the first to examine
disease activity as control variables (Table 5). Multivariate asymptomatic myocardial dysfunction in drug-naïve patients
regression analysis showed that hsCRP level and epicardial with new-onset SLE via a speckle-tracking-based multilayer
GLS are the predictors of layer-specific GLS impairment approach. The main findings are that decreased whole
and PSD change, respectively (Table 6). layer GLS, endocardial GLS, and epicardial GLS could be
found in SLE patients, when compared with age- and sex-
matched healthy individuals. This suggests that subclinical
Intra- and inter-observer variability of GLS
impairment of left ventricular function can occur as early as
Intra-observer variabilities and inter-observer reliability for the time when SLE is newly diagnosed and LVEF remains
whole GLS, endocardial GLS, and epicardial GLS were preserved.
analyzed by a Bland-Altman plot presented (Figure 4), and Interestingly, SLE patients had impaired myocardial
were all within the limits of agreement. GLS but not GCS. The relationship between LS and CS is
© Quantitative Imaging in Medicine and Surgery. All rights reserved. Quant Imaging Med Surg 2021;11(4):1271-1283 | http://dx.doi.org/10.21037/qims-20-8591276 Luo et al. Layer-specific speckle-tracking scan in SLE patients Apical 4-chamber view Apical 2-chamber view Apical 3-chamber view Figure 1 Typical layer-specific global longitudinal strain (GLS) images of the left ventricle (LV) from a patient with systemic lupus erythematosus (left) and a healthy individual (right). LV GLS was measured from three different views [apical 4 (upper level images)-, 2 (middle level images)-, and 3 (bottom level images)-chamber views]. Measurement of whole layer GLS, endocardial GLS, and epicardial GLS were performed. still not clear. Emerging evidence shows that different roles patients. are played by CS and LS in left ventricular ejection (14), PSD has been proven to be a relatively new and useful with circumferential shortening contributing more to LVEF marker for the early detection of LVMD (17,18). Mounting (14,15). In contrast, patients with impaired longitudinal evidence suggests that LVMD has an independent and shortening constantly have preserved LVEF. This result was incremental negative impact on myocardial mechanics and also consistent with the study by Kraigher-Krainer et al. who remodeling. In the study by Leong et al., left ventricular found that in heart failure with preserved ejection fraction (LV) dyssynchrony was independently associated with (HFpEF), after adjustment for 10 baseline covariates, lower changes in the LVEF over time in idiopathic dilated LS but not CS was associated with higher NT-proBNP, a cardiomyopathy and the occurrence of ventricular prognostically relevant biomarker in HFpEF (16). In our tachycardia after myocardial infarction (19). Fudim et al. study, decreased GLS was found in new-onset SLE patients demonstrated that LV dyssynchrony was strongly associated with normal LVEF, suggesting GLS might be a marker with adverse outcomes among patients with coronary heart for the early detection of myocardial dysfunction in SLE disease (20). In our study, elevation of PSD was detected © Quantitative Imaging in Medicine and Surgery. All rights reserved. Quant Imaging Med Surg 2021;11(4):1271-1283 | http://dx.doi.org/10.21037/qims-20-859
Quantitative Imaging in Medicine and Surgery, Vol 11, No 4 April 2021 1277 GCS at apical level GCS at papillary muscle level GCS at basal level Figure 2 Representative plot of layer-specific global circumferential strain (GCS) in the left ventricle (LV) of an SLE patient (left) and a healthy individual (right). LV GCS was measured from three different levels (apical level, papillary muscle level, and basal level). Measurement of midmyocardium GCS, endocardium GCS, and epicardium GCS were performed. in drug-naïve SLE patients for the first time, suggesting (24-26). Similarly, our results showed that more active subclinical LVMD in SLE. Moreover, previous studies disease, high-risk aPL profile, renal involvement, and have shown that LVMD was particularly prevalent in higher hsCRP level were linked with the tendency towards patients with microvascular involvement (21), which is more severe; 7 impaired GLS parameters and higher PSD also a characteristic lesion mediated by immune complex (although not always with statistical significance). Active deposition in SLE. Whether or not higher PSD predicts a disease is associated with macrophage activation, which poorer myocardial prognosis in patients with SLE needs to enhances the pro-inflammatory process of CVD occurrence be clarified in further research. in SLE (27). A high-risk aPL profile not only mediates Both mouse models and clinical evidence have hypercoagulable states and endothelial dysfunction, but shown that lupus-associated risk factors play key roles also exacerbates atherosclerosis inflammation in SLE with in the pathogenesis of cardiovascular disease (CVD) in antiphospholipid syndrome (28). Gustafsson et al. reported SLE patients (22,23). Disease activity, inflammation, that accelerated atherosclerosis in SLE is mainly confined antiphospholipid antibody, and lupus nephritis are among to a subgroup with lupus nephritis (29). The four factors the most studied SLE-associated cardiovascular risk factors above may work alone or coordinate to cause LS and PSD © Quantitative Imaging in Medicine and Surgery. All rights reserved. Quant Imaging Med Surg 2021;11(4):1271-1283 | http://dx.doi.org/10.21037/qims-20-859
1278 Luo et al. Layer-specific speckle-tracking scan in SLE patients Table 3 Layer-specific strain data and left ventricular dyssynchrony index parameters in SLE patients and controls Variables SLE Healthy controls P Whole layer GLS (%) −17.6±3.0 −19.3±2.6 0.02 Endocardial GLS (%) −20.0±3.2 −22.1±3.0 0.01 Epicardial GLS (%) −15.6±2.7 −16.8±2.4 0.04 GCS at basal level Endocardium (%) −25.6±6.3 −24.4±6.0 0.458 Mid-myocardium (%) −18.0±4.4 −16.9±4.5 0.376 Epicardium (%) −12.8±4.0 −12.2±3.9 0.675 GCS at papillary muscle level Endocardium (%) −29.0±5.5 −27.1±7.0 0.239 Mid-myocardium (%) −20.3±3.9 −18.3±5.3 0.124 Epicardium (%) −14.2±4.5 −12.5±4.3 0.136 GCS at apical level Endocardium (%) −33.8±5.7 −32.7±8.4 0.605 Mid-myocardium (%) −23.4±4.9 −22.5±6.3 0.686 Epicardium (%) −16.0±5.6 −15.5±5.9 0.708 PSD (msec) 41.0±18.9 28.8±10.1 0.007 STE, speckle-tracking echocardiography; GCS, global circumferential strain; GLS, global longitudinal strain; PSD, peak systolic dispersion. Table 4 Layer-specific longitudinal parameters, PSD, and certain disease-related contributors of cardiovascular risk in SLE patients Variable Whole layer GLS (%) Endocardial GLS (%) Epicardial GLS (%) PSD (msec) Disease activity Inactive-to-mild active disease −19.3±2.3 −21.8±2.6 −17.1±2.2 34.1±16.1 Moderate-to-severe active −15.8±2.5 −18.1±2.8 −13.9±2.3 48.2±19.3 disease P
Quantitative Imaging in Medicine and Surgery, Vol 11, No 4 April 2021 1279
0 0 100 r=0.390 0
Endocardial GLS (%)
r=0.662 r=0.637 r=0.658
Epicardial GLS (%)
P=0.021
GLS in whole (%)
P1280 Luo et al. Layer-specific speckle-tracking scan in SLE patients
Table 6 Multivariate linear regression to analyze predictors of layer-specific GLS parameters and PSD
Unstandardized coefficients Standardized coefficients
Model p
B Std. error Beta t
Whole layer GLS
Constant −21.725 0.815 −26.656Quantitative Imaging in Medicine and Surgery, Vol 11, No 4 April 2021 1281
Intraobserver (investigator A) Intraobserver (investigator B) Intraobserver (investigator A-B)
4 5 6
3 4
Difference of whole GLS (%)
Difference of whole GLS (%)
4
Difference of whole GLS (%)
2 3
2
1 2
1
0
0 0
–1
–1
–2 –2
–2
–3 –3
–4
–4 –4
–5 –5 –6
10 15 20 25 30 10 15 20 25 30 10 15 20 25 30
Average of whole GLS (%) Average of whole GLS (%) Average of whole GLS (%)
Intraobserver (investigator A) Intraobserver (investigator B) Intraobserver (investigator A-B)
6 8 6
Difference of endocardial GLS (%)
Difference of endocardial GLS (%)
Difference of endocardial GLS (%)
4 6 4
2 4
2
0 2
0
–2 0
–2
–4 –2
–6 –4 –4
–8 –6 –6
10 15 20 25 30 35 10 15 20 25 30 35 10 15 20 25 30 35
Average of endocardial GLS (%) Average of endocardial GLS (%) Average of endocardial GLS (%)
Intraobserver (investigator A) Intraobserver (investigator B) Intraobserver (investigator A-B)
4 6 4
Difference of epicardial GLS (%)
Difference of epicardial GLS (%)
Difference of epicardial GLS (%)
3
4 3
2
2
1 2
0 1
0
–1 0
–2 –2
–1
–3
–4 –2
–4
–5 –6 –3
10 12 14 16 18 20 22 24 5 10 15 20 25 10 12 14 16 18 20 22 24
Average of epicardial GLS (%) Average of epicardial GLS (%) Average of epicardial GLS (%)
Figure 4 Bland-Altman analysis of (I) intra-observer reliability for whole global longitudinal strain (GLS), endocardial GLS, and epicardial
GLS of two investigators (left and middle); (II) interobserver reliability of whole GLS, endocardial GLS, and epicardial GLS (right).
Acknowledgments Hospital of Fujian Medical University.
Funding: This work was supported by Key Clinical Specialty
Open Access Statement: This is an Open Access article distributed
Discipline Construction Program of Fujian, China,
in accordance with the Creative Commons Attribution-
Natural Science Foundation of Fujian Province (grant No.
NonCommercial-NoDerivs 4.0 International License (CC BY-
2019J01473) and the Science and Technology Program of NC-ND 4.0), which permits the non-commercial replication
Quanzhou (grant No. 2018N014S, 2017Z009). and distribution of the article with the strict proviso that no
changes or edits are made and the original work is properly
Footnote cited (including links to both the formal publication through the
relevant DOI and the license). See: https://creativecommons.
Conflicts of Interest: All authors have completed the ICMJE org/licenses/by-nc-nd/4.0/.
uniform disclosure form (available at http://dx.doi.
org/10.21037/qims-20-859). The authors have no conflicts
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Cite this article as: Luo T, Wang Z, Chen Z, Yu E, Fang C.
Layer-specific strain and dyssynchrony index alteration in new-
onset systemic lupus erythematosus patients without cardiac
symptoms. Quant Imaging Med Surg 2021;11(4):1271-1283.
doi: 10.21037/qims-20-859
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